Published on Web 01/04/2006
Models of the Membrane-Bound Cytochromes: Mo1 ssbauer Spectra of Crystalline Low-Spin Ferriheme Complexes Having Axial Ligand Plane Dihedral Angles Ranging from 0° to 90° Thomas Teschner,‡ Liliya Yatsunyk,† Volker Schu¨nemann,*,‡,| Hauke Paulsen,‡ Heiner Winkler,‡ Chuanjiang Hu,# W. Robert Scheidt,# F. Ann Walker,*,† and Alfred X. Trautwein*,‡ Contribution from the Institut fu¨r Physik, UniVersita¨t zu Lu¨beck, Ratzeburger Allee 160 D-23538 Lu¨beck, Germany, Department of Chemistry, The UniVersity of Arizona, Tucson, Arizona 85721-0041, Fachbereich Physik, Technische UniVersita¨t Kaiserslautern, Erwin-Schro¨dinger-Strasse 56, D-67663 Kaiserslautern, Germany, and Department of Chemistry and Biochemistry, UniVersity of Notre Dame, Notre Dame, Indiana 46556-5670 Received September 14, 2005; E-mail:
[email protected];
[email protected];
[email protected] Abstract: Crystalline samples of four low-spin Fe(III) octaalkyltetraphenylporphyrinate and two low-spin Fe(III) tetramesitylporphyrinate complexes, all of which are models of the bis-histidine-coordinated cytochromes of mitochondrial complexes II, III, and IV and chloroplast complex b6 f, and whose molecular structures and EPR spectra have been reported previously, have been investigated in detail by Mo¨ssbauer spectroscopy. The six complexes and the dihedral angles between axial ligand planes of each are [(TMP)Fe(1-MeIm)2]ClO4 (0°), paral-[(OMTPP)Fe(1-MeIm)2]Cl (19.5°), paral-[(TMP)Fe(5-MeHIm)2]ClO4 (26°, 30° for two molecules in the unit cell whose EPR spectra overlap), [(OETPP)Fe(4-Me2NPy)2]Cl (70°), perp[(OETPP)Fe(1-MeIm)2]Cl (73°), and perp-[(OMTPP)Fe(1-MeIm)2]Cl (90°). Of these, the first three have been shown to exhibit normal rhombic EPR spectra, each with three clearly resolved g-values, while the last three have been shown to exhibit “large gmax” EPR spectra at 4.2 K. It is found that the hyperfine coupling constants of the complexes are consistent with those reported previously for low-spin ferriheme systems, with the largest-magnitude hyperfine coupling constant, Azz, being considerably smaller for the “parallel” complexes (400-540 kG) than for the strictly perpendicular complex (902 kG), Axx being negative for all six complexes, and Azz and Axx being of similar magnitude for the “parallel” complexes (for example, for [(TMP)Fe(1-MeIm)2]Cl, Azz ) 400 kG, Axx ) -400 kG). In all cases, Ayy is small but difficult to estimate with accuracy. With results for six structurally characterized model systems, we find for the first time qualitative correlations of gzz, Azz, and ∆EQ with axial ligand plane dihedral angle ∆φ.
Introduction
Heme-containing electron-transfer proteins are essential to many biological processes. The two major classes of hemebased electron-transport proteins, having bis-histidine- and histidine-methionine-coordinated heme centers, shuttle between iron(II) and iron(III) oxidation states and are usually called the cytochromes a, b, and c, based on the differing substituents on the periphery of the heme. In addition to relatively small molecular weight heme proteins,1-9 a number of cytochrome‡
Universita¨t zu Lu¨beck. The University of Arizona. | Technische Universita ¨ t Kaiserslautern. # University of Notre Dame. †
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ARTICLES
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gmax” 39 type with gmax ) 3.41-3.44 and 3.75-3.78 for high and low reduction potential hemes, bH and bL, respectively. Cytochrome b6 f does not yield a resolved EPR signal for the hemes of cytochrome b6 (except for the high-spin heme sometimes called heme x40), but the g-values of hemes bl and bh (also called bn and bp) have been estimated as 3.6 by magnetic Mo¨ssbauer spectroscopy.41 For the cytochrome bc1 complex of mitochondria and the structurally and functionally related cytochrome b6 f complex of chloroplasts, these “large gmax” EPR signals “relax” to normal rhombic EPR signals (with g1, g2, and g3 values observed, and typically 2.9, 2.25, and 1.54, respectively) when the cytochrome b protein is extracted from the membrane and the other proteins of the complex.42-44 In earlier work with bis-imidazole-ligated iron(III) porphyrinates, we have found that the axial ligand arrangement, i.e., the absolute and relative orientations of the two planar axial ligands, is an important factor in defining the EPR spectroscopic properties.39,45-48 Ligand orientation is also likely to be a significant determinant of the reduction potentials of these heme centers. Studies with synthetic ferriheme complexes have shown that the coordination of bulky imidazoles (2-methylimidazole, 1,2-dimethylimidazole, etc.) or some pyridines (3,4-dimethylamino-pyridine, pyridine itself, etc.) to iron(III) tetraphenylporphyrin (TPPFe(III))39,45 or hemin itself ((ProtoIX)Fe(III))49,50 leads to a “large gmax” EPR signal similar to that reported for the bc1 complex.37,38 These signals have one g value g3.2 (sometimes as large as 3.78) and nearly or completely undetectable g2 and g3, and are observable only at very low temperature (
